Oecologia Australis 23(1): 145–149, 2019 https://doi.org/10.4257/oeco.2019.2301.13

STOMACH CONTENT ANALYSIS OF noctivagus noctivagus (TINAMIFORMES, TINAMIDAE) IN SOUTHERN BRAZIL

Luiz Liberato Costa Corrêa1*& Maria Virginia Petry1

1 Universidade do Vale do Rio dos Sinos, Programa de Pós-Graduação em Biologia, Laboratório de Ornitologia e Animais Marinhos, Av. Unisinos, nº 950, Bairro Cristo Rei, CEP 93022-750, São Leopoldo, RS, Brazil.

E-mails: [email protected] (*corresponding author); [email protected]

Abstract: Studies reporting specific aspects of forest ’ feeding ecology are still scarce in the scientific literature, and most of the available information report only casual observations. The Crypturellus noctivagus noctivagus (Tinamiformes, Tinamidae) is a forest endemic to Brazil, which occurs from southern Bahia to Rio Grande do Sul. In this study, we analyzed food items found in the stomach content of one C. n. noctivagus individual in the state of Rio Grande do Sul, Brazil. We found seeds of Nectandra megapotamica (Laurales, Lauraceae) and Myrcianthes gigantea (Myrtales, Myrtaceae), totalizing 2.259 g. We also found insect fragments of the orders Coleoptera and Lepidoptera, one individual of the family Curculionidae (Coleoptera), and one larval specimen of Dirphia muscosa (Lepdoptera), totalizing 0.637 g of stomach content, and rock fragments weight 1.741 g. This study provides records of the C. n. noctivagus feeding habits, contributing to the knowledge about the trophic ecology of Tinamiformes in South Brazil.

Keywords: Pampa Biome; Seasonal deciduous forest; Tinamiformes; Yellow-legged .

The Yellow-legged Tinamou Crypturellus noctivagus noctivagus is classified as Critically Endangered at (Wied, 1820) is a forest bird endemic to Brazil, the regional level (FZB 2014). included in the Tinamiformes (BirdLife The Yellow-legged Tinamou has terrestrial International 2016). In regard to conservation habits, using the ground to displace and to attend status, the species is considered as Vulnerable at its trophic demands (Magalhães 1994, BirdLife the national level (ICMBIo 2016). Two subspecies International 2016), foraging on fallen fruits, bugs are recognized: Crypturellus noctivagus zabele and ants (Berlepsch & Ihering 1885, Sick 1997). (Spix, 1825), found in the North portion of the Some field studies report specific food items in the states of Bahia, Piauí and possibly Pernambuco, diet of wild tinamous, such as maculosa and Crypturellus noctivagus noctivagus (Wied, (Silva & Sander 1981), Nothura pentlandii (Mosa 1820) which occurs from South Bahia, following 1993) and perdicaria (González-Acuña southwards by the coastal region, through Atlantic et al. 2006). Regarding forest tinamous (e.g., species Forest remnants (Magalhães 1994, BirdLife of the Crypturellus), information about International 2016, Tomotani & Silveira 2016), to the specific food habits are still scarce in the literature. Pampa Biome in the Rio Grande do Sul state, where In general, these are known to feed on fruits, only one relictual population is known (Corrêa seeds, arthropods and fruit pulps available on the et al. 2010). In the Rio Grande do Sul state, C. n. ground (Sick 1984, Cabot 1992). Forest birds which 146 | Stomach content analysis of Crypturellus n. noctivagus feed on fruits and seeds may, directly or indirectly, contribute to seed dispersion in the ecosystem, carrying seeds trough both flight and ground displacements (Andrade 1997, Sick, 1997, Pizo & Galetti 2010). Several bird groups play such role in forest environments, such as the families Cracidae, Psittacidae, Tyrannidae, Turdidae and Thraupidae (Sick 1984, Aspiroz 2001, Krügel et al. 2006, Pizo & Galetti 2010), as well as many species of the family Tinamidae (Cabot 1992), thus providing an ecosystem service. Considering the lack of information regarding the diet and feeding habits of the Yellow-legged Tinamou, in this study we aimed to analyze the stomach content of C. n. noctivagus and to identify food items at specific level, in order to contribute to the knowledge about Tinamidae trophic ecology in seasonal deciduous forest. The study area is located in a forest fragment (30°05’35.3”S, 53°36’22.9”W) between the municipalities of São Sepé and Formigueiro (Figure 1), central portion of the Rio Grande do Sul state, Brazil (Corrêa et al. 2010). The Figure 1. Study area, forest remnant with about region climate is considered as temperate, with an 450 ha located between São Tepé and Formigueiro municipalities, in the Pampa Biome, Rio Grande do average annual temperature of 19°C and average Sul state, Brazil. annual precipitation of 1,750mm (Alvares et al. 2013). The region belongs to the Pampa Biome and dishes, and identified using a stereomicroscope. presents seasonal deciduous forest, and is under Items were separated into the following categories: intense anthropogenic pressure due to the expansion arthropods, seeds and rock fragments. For arthropod of the agriculture frontier (IBGE 2004). identification we followed Spechtet al. (2008) Between 2015 and 2016, we conducted field work and Triplehorn & Johnson (2011). In the following in order to collect ecological information of C. n. year, 2017, during the same season when the C. n. noctivagus in the study area. In November 2016, when noctivagus specimen was collected, we randomly individuals were captured using a bell-trap (Corrêa & searched for fruits and seeds on the ground in Petry 2018) and manipulated by researchers in order the study area, for further comparison with the to collect biological samples, one specimen (adult vegetable items found in the stomach content. We female) came to death. The specimen was frozen followed Longhi (1995), Lorenzi (2000) and Backes and brought to the Laboratório de Ornitologia e & Irgang (2002) for fruit and seed identification. All Animais Marinhos at the Universidade do Vale do Rio food items were quantified and weighed using a dos Sinos, Rio Grande do Sul state, Brazil. Then, the precision balance Bel-modelo MARK M 1003. The specimen was deposited in the scientific collection capture techniques were both approved by System of the Museu de Zoologia of the Universidade do of Authorization and Information of Biodiversity Vale do Rio dos Sinos (MZU-973). The specimen (SISBIO, № 47126‑3) and by the Ethics Committee presented the following measures: 29.53 mm of bill on the Use of in Research (CEUA, number length, 65.51 mm of head length, 59.22 mm of tarsus PPECEUAI0.2014), Universidade do Vale do Rio dos length, 180 mm of wing length, 60 mm of tail length, Sinos. 333 mm of total body length and 670 g of total body Plant items were found, composed by seeds mass. of Lauraceae (Nectandra megapotamica) and The stomach content was removed from the Myrtaceae (Myrcianthes gigantea). Two seeds ventriculus and proventriculus of the specimen and and a few fragments were not possible to identify. separated into categories, using tweezers and Petri Seeds were the most representative items in the

Oecol. Aust. 23(1): 145–149, 2019 Corrêa & Petry | 147 stomach content of C. n. noctivagus, specially these seasons coincides with the species breeding N. megapotamica (1.773 g). We found two insect period, when the energy demands of individuals Orders in the diet of C. n. noctivagus: Coleoptera are higher in order to perform courtship, egg laying, and Lepidoptera, besides fragments of insects of the incubation and chick rearing (e.g., Sick 1984, Cabot same Orders which were not possible to identify at a 1992). specific level. We found one specimen of the family The Yellow-legged Tinamou provides important Curculionidae, order Coleoptera. Representing the ecosystem services, since it is considered a seed Order Lepidoptera, one larval specimen of Dirphia disperser due to the great amount of seeds found muscosa (Family Saturniidae) was identified. Rock in the species diet, along with the high capacity of fragments were also found (Table 1). locomotion within the forest, thus promoting seed Regarding vegetable items, N. megapotamica dispersion over long distances. It is known that was the predominant species in the diet of this C. forest tinamous present great viewing capacity, n. noctivagus specimen. According to Krügel et al. using this sense to explore foraging environments, (2006), in a study conducted in the Rio Grande do searching for fruits, seeds and potential prey on Sul state, N. megapotamica fruits were consumed the ground (Cabot 1992, Sick 1997). Frugivorous by bird species that forage during flight (e.g., birds explore a wide variety of fruits, which may be Tyrannidae and Trogonidae), and also by those available on the ground or in the trees, according to that forage landed (e.g., Cracidae, Psittacidae and the period, in order to attend its trophic demands Emberizidae), especially during spring and summer, (Andrade 1997, Sick 1997, Pizo & Galetti 2010). Fruits which comprises the fruiting period. Therefore, N. of N. megapotamica are about 1.5 cm length, when megapotamica may represents an important food ripe are aromatic and attractive, presenting reddish resource for the avifauna (Frisch & Frisch 2005), thus coloration. Each fruit presents one seed, which contributing to the forest ecosystem maintenance is greenish/brownish (Longhi 1995). Myrcianthes through consumer-resource interactions. To a lesser gigantea fruits, when ripe, are about 1 cm length, extent, among vegetable items, we found M. gigantea reddish, and may contain up to two seeds of composing the diet of C. n. noctivagus. Myrcianthes yellowish tones (Lorenzi 2000, Backes & Irgang 2002). gigantea is also an abundant species in the central Our results corroborate such information, since the portion of the state of Rio Grande do Sul, presenting vegetable items found in the stomach content of C. fruiting period between spring and summer (Longhi n. noctivagus were derived from reddish-colored 1995). The presence of this species in the stomach fruits. Fruits of both species fall on the ground when content indicates that, during this period of the year, reach maturity (Longhi 1995, Backes & Irgang 2002), it represents an important food resource for large becoming a foraging resource for the terrestrial local birds such as C. n. noctivagus. Especially because fauna.

Table 1. Food items found in the stomach content of Crypturellus noctivagus noctivagus (Tinamiformes, Tinamidae) in the Rio Grande do Sul state. UN = Number of items; BI =total biomass in each category.

Category Order Family Species UN BI (g) Seeds Myrtales Myrtaceae Myrciathes gigantea 05 0.250 Laurales Lauraceae Nectandra 30 1.773 megapotamica Undetermined 02 0.100 Seeds fragments Undetermined 09 0.136 Insects Lepidoptera Saturniidae Dirphia muscosa 01 0.608 Undetermined 05 frag. 0.002 Coleoptera Curculionidae Undetermined 01 0.020 Insect fragmens Undetermined 12 0.007 Rock fragments 54 1.741

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During the breeding season, when a higher ACKNOWLEDGMENTS energy demand is required, some bird species may complement their diets by feeding on invertebrates/ We would like to thank the colleagues from the arthropods, being considered as opportunistic Laboratório de Ornitologia e Animais Marinhos frugivorous (Krügel et al. 2006). The low arthropod (UNISINOS), especially Douglas R. da Silva and biomass found in our study for this single specimen Renata Brentano or technical support. This study indicates that invertebrates were consumed as was financed in part by the Coordenação de supplementary resources, which suggests that the Aperfeiçoamento de Pessoal de Nível Superior - Yellow-legged Tinamou is a large frugivorous bird. Brasil (CAPES) - Finance Code 001. Finally, to the However, it is important to investigate the diet of reviewers. other specimens to infer such conclusion. Bugs of the family Curculionidae feed on live and dead plants and REFERENCES adult individuals may penetrate and remain within fruits for a certain time (Triplehorn & Johnson 2011). Alvares, C. A, Stape, J. L., Sentelhas, P. C., Gonçalves, Considering that the Yellow-legged Tinamou forages J. L., & Sparovek, G. 2013. Köppen’s climate on the ground (Berlepsch & Ihering 1885, Sick 1984), classification map for Brazil. Meteorologische it is possible that the bug found in the stomach Zeitschrift, 22(6), 711–728. DOI: 10.1127/0941- content was ingested as an indirect resource, along 2948/2013/0507 with a consumed fruit, or even among the litter. Andrade, M. A. 1997. A vida das aves: introdução Lepidoptera, even in low occurrence, was present in à biologia e conservação. Belo Horizonte: the diet of C. n. noctivagus, represented by one larval Fundação Acangaú Líttera: p.160. specimen of D. muscosa. It is an abundant species Aspiroz, A. B. 2001. Aves del Uruguay. Lista e in southern Brazil, which uses native and/or exotic introducción a su biología y conservación. plants as hosts during larval development (Specht Montevideo: Aves Uruguay, GUPECA: p.104. et al. 2005, Specht et al. 2008). Most caterpillars of Backes, P., & Irgang, B. 2002. Árvores do Sul: guia de this group become pupae in silk chrysalises fixed in identificação & interesse ecológico – as principais leaves on the trees, although some species becomes espécies nativas sul-brasileiras. Santa Cruz do pupae in leaves on the ground (Specht et al. 2008, Sul: Clube da Árvore, Instituto Souza Cruz: p.325. Triplehorn & Johnson 2011), where it probably has Berlepsch, H. V., & Ihering, H. V. 1885. Die Vögel der been ingested by C. n. noctivagus. Rock fragments Umgegend von Taquara do Mundo Novo, Prov. presented the second largest mass among all items Rio Grande do Sul. Zeitschr gesammte Ornith, 2, found in the stomach content. The ingestion of such 97–184. fragments by birds improves the digestive process by Birdlife International. 2016. Species factsheet: aiding the trituration of food items. The behavior of Crypturellus noctivagus. IUCN Red List of ingesting rocks is common in tinamous species due Threatened Species. Retrieved on January 05, to the habit of such birds of feeding on seeds (Cabot 2018. Avaliable at: http://www.iucnredlist. 1992, Sick 1997). org/details/22678217/0. DOI: 10.2305/IUCN. Among forest birds, large frugivorous such as UK.2016-3.RLTS.T22678217A92761578.en the Yellow-legged Tinamou are among the most Cabot, J. 1992. Order Tinamiformes. In: J. Del Hoyo, threatened species (Sick 1984, Cabot 1992), since A. Elliott, & J. Sargatal (Eds.), Handbook of the they need fruit availability over the whole year birds of the world. pp. 112–125. Barcelona: Lynx (Willis 1979, Gray et al. 2007). Thus, management Editions. measures are extremely needed for the conservation Corrêa, L. L. C, Silva, D. E., & Cappellari, L. H. of frugivorous biodiversity in forest remnants in the 2010. Aves, Tinamidae, Crypturellus noctivagus Rio Grande do Sul state. In our study, C. n. noctivagus noctivagus (Wied, 1820): southward range presented a seed-based diet, specially derived from extension and rediscovery in Rio Grande N. megapotamica fruits, as well as arthropods as do Sul, Brazil. ChekList, 6(4). 485–486. DOI: complementary resources. 10.15560/6.4.585 Corrêa, L. L. C., & Petry, M.V. 2018. Testing capturing

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